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Natural Diversity in the Predatory Behavior Facilitates the Establishment of a Robust Model Strain for Nematode-Trapping Fungi

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Natural Diversity in the Predatory Behavior Facilitates the Establishment of a Robust Model Strain for Nematode-Trapping Fungi Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi Ching-Ting Yanga,1, Guillermo Vidal-Diez de Ulzurruna,1, A. Pedro Gonçalvesa, Hung-Che Lina,b, Ching-Wen Changa,c, Tsung-Yu Huanga, Sheng-An Chena, Cheng-Kuo Laid, Isheng J. Tsaid, Frank C. Schroedere,f, Jason E. Stajichg, and Yen-Ping Hsueha,b,c,2 aInstitute of Molecular Biology, Academia Sinica, Nangang, Taipei 115, Taiwan; bGenome and Systems Biology Degree Program, National Taiwan University and Academia Sinica, Taipei 106, Taiwan; cDepartment of Biochemical Science and Technology, National Taiwan University, Taipei 106, Taiwan; dBiodiversity Research Center, Academia Sinica, Nangang, Taipei 115, Taiwan; eBoyce Thompson Institute, Cornell University, Ithaca, NY 14853; fDepartment of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853; and gDepartment of Microbiology and Plant Pathology, University of California, Riverside, CA 92521 Edited by Iva Greenwald, Columbia University, New York, NY, and approved February 5, 2020 (received for review November 9, 2019) Nematode-trapping fungi (NTF) are a group of specialized microbial the induction of trap morphogenesis (7), and that NTF use predators that consume nematodes when food sources are limited. olfactory mimicry to lure their prey into traps (8). Upon being Predation is initiated when conserved nematode ascaroside pher- trapped, the nematodes are paralyzed, pierced, invaded, and omones are sensed, followed by the development of complex digested by the fungus (5, 6). Both nematodes and NTF can be trapping devices. To gain insights into the coevolution of this found in a wide range of habitats (9, 10); however, sympatrism – interkingdom predator prey relationship, we investigated natural and adaptation in the context of their relationship are yet to be populations of nematodes and NTF that we found to be ubiqui- investigated and little is known about the natural history of this tous in soils. Arthrobotrys species were sympatric with various example of a predator–prey interaction. nematode species and behaved as generalist predators. The ability In this study, we investigated the ecology of natural populations to sense prey among wild isolates of Arthrobotrys oligospora var- of nematodes and NTF and found that Arthrobotrys species were ied greatly, as determined by the number of traps after exposure sympatric with diverse nematodes and behaved as generalist MICROBIOLOGY to Caenorhabditis elegans. While some strains were highly sensi- tive to C. elegans and the nematode pheromone ascarosides, others responded only weakly. Furthermore, strains that were Significance highly sensitive to the nematode prey also developed traps faster. The polymorphic nature of trap formation correlated with compe- Nematode-trapping fungi (NTF) are carnivorous microbes that tency in prey killing, as well as with the phylogeny of A. oligospora hold potential to be used as biological control agents due to natural strains, calculated after assembly and annotation of the their ability to consume nematodes. In this work, we show that genomes of 20 isolates. A chromosome-level genome assembly NTF are ubiquitous generalist predators found in sympatry and annotation were established for one of the most sensitive with their prey in soil samples. Wild isolates of NTF displayed a wild isolates, and deletion of the only G-protein β-subunit– naturally diverse ability to execute their predatory lifestyle. We encoding gene of A. oligospora nearly abolished trap formation. generated a large whole-genome sequencing dataset for many In summary, our study establishes a highly responsive A. oligospora of the fungal isolates that will serve as the basis of future wild isolate as a model strain for the study of fungus–nematode projects. In particular, we establish TWF154, a highly respon- interactions and demonstrates that trap formation is a fitness sive strain of Arthrobotrys oligospora, as a model strain to character in generalist predators of the nematode-trapping fungus study the genetics of NTF. Lastly, we provide evidence that the family. G-protein β-subunit Gpb1 plays an important role in trap in- duction in NTF. nematode-trapping fungi | predator–prey interaction | natural population | G-protein signaling | trap morphogenesis Author contributions: C.-T.Y., G.V.-D.d.U., and Y.-P.H. designed research; C.-T.Y., G.V.-D.d.U., H.-C.L., C.-W.C., T.-Y.H., S.-A.C., and Y.-P.H. performed research; H.-C.L., C.-W.C., S.-A.C., F.C.S., J.E.S., and Y.-P.H. contributed new reagents/analytic tools; C.-T.Y., G.V.-D.d.U., A.P.G., H.-C.L., he living components of soils are in permanent interaction C.-W.C., T.-Y.H., C.-K.L., I.J.T., and Y.-P.H. analyzed data; and G.V.-D.d.U., A.P.G., S.-A.C., and Tand play central roles in various aspects of biogeochemistry, Y.-P.H. wrote the paper. including nutrient cycling and transport across distances (1). The authors declare no competing interest. Specifically, nematodes are the most abundant animals in nature, This article is a PNAS Direct Submission. 20 amounting to a staggering 0.3 gigatonnes or 4.5 × 10 individ- Published under the PNAS license. uals, many of which are devastating parasites of plants, animals, Data deposition: The genomic data presented in this paper have been deposited to and humans (2). Although available, nematicide chemicals pose National Center for Biotechnology Information GenBank. The accession numbers are severe environmental and health risks and therefore biological SOZJ00000000 (TWF154 reference genome), MN972613 (TWF154 mitochondria), WIQW00000000 (TWF102), WIQX00000000 (TWF103), WIWS00000000 (TWF106), control agents such as carnivorous predatory fungi hold potential JAABOH000000000 (TWF128), JAABLO000000000 (TWF132), JAAGKP000000000 (TWF173), as alternative pest control tools. Predatory fungi that prey and WIPF00000000 (TWF191), WIPG00000000 (TWF192), JAABOI000000000 (TWF217), consume nematodes have been described from several major WIWR00000000 (TWF225), WIRA00000000 (TWF569), WIRB00000000 (TWF594), WIWT00000000 (TWF679), WIQZ00000000 (TWF703), WIQY00000000 (TWF706), fungal phyla, suggesting that fungal carnivorism has arisen in- WIWQ00000000 (TWF751), JAABOE000000000 (TWF788), and JAABOJ000000000 dependently multiple times during evolution (3, 4). In partic- (TWF970). References to these accession numbers can also be found throughout this paper ular, nematode-trapping fungi (NTF) constitute a group of and in SI Appendix. nematophagous organisms that includes a large number of species 1C.-T.Y. and G.V.-D.d.U. contributed equally to this work. that rely on the formation of traps to ambush their prey (5, 6). We 2To whom correspondence may be addressed. Email: [email protected]. have previously described that NTF eavesdrop on an evolutionarily This article contains supporting information online at https://www.pnas.org/lookup/suppl/ conserved family of nematode pheromones, the ascarosides, that doi:10.1073/pnas.1919726117/-/DCSupplemental. are used as a signal to switch from saprophytism to predation via www.pnas.org/cgi/doi/10.1073/pnas.1919726117 PNAS Latest Articles | 1of9 Downloaded by guest on September 24, 2021 predators. The degree of predation varied greatly among strains vast majority of the 178 soil samples and ∼92 and ∼68% of the and several wild isolates were substantially more efficient pred- sampling sites contained nematodes and/or NTF, respectively. ators than the currently used laboratory strain. We sequenced They were sympatric in more than 63% of the sites, indicating that and assembled the genomes of a number of wild Arthrobotrys these organisms share the same niches in soil environments and oligospora strains and demonstrated a correlation between the interact closely in nature (Fig. 1B). Only 2 sampling sites (the levels of trap formation, prey killing efficiency, and phylogeny. Xiaoyoukeng fumarole at Yangmingshan National Park and the Lastly, targeted gene deletion of a vG-protein β-subunit–encoding coastline of Penghu Island) were found to be free of nematodes gene revealed that the predatory lifestyle of A. oligospora is de- and NTF, presumably due to extreme environments (high tem- pendent upon G-protein signaling. perature and high salt concentration, respectively) that likely impede survival. In total, we identified 16 previously described Results and Discussion species of NTF, as well as a few strains that could represent new Soil Samples Reveal a Rich Diversity of Nematodes and NTF. With the species. Among the 16 known species, 11 were identified as goal of isolating sympatric nematodes and NTF from natural belonging to the genus Arthrobotrys, which develops 3D adhesive habitats, we collected 178 soil samples from 69 ecologically diverse nets as a trapping device to capture prey (5, 6) (Fig. 1C). A. sites in Taiwan (Fig. 1A). Sampling sites were mainly located in oligospora was the most commonly found species, followed by northern and central Taiwan, and included forest, lake, agricul- Arthrobotrys thaumasia and Arthrobotrys musiformis; combined, tural, and coastal environments as well as educational campuses. these 3 species were present in ∼70% of the sampling sites that More than 66% of the sampling sites were mountainous areas, had been identified as harboring NTF (Fig. 1C). The remaining with altitudes ranging from ∼300 to 3,400 m (SI Appendix,Table 5 species were of the Monacrosporium and Drechslerella genera, S3). We established pure cultures of both organisms and
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